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Adulteration of Selected Unprocessed Botanicals in the U.S.

Retail Herbal Trade1


KAREN M. WALKER*
AND

WENDY L. APPLEQUIST

William L. Brown Center, Missouri Botanical Garden, P.O. Box 299St. Louis, MO 63166-0299, USA *Corresponding author; e-mail: karen.walker@mobot.org

Adulteration of Selected Unprocessed Botanicals in the U.S. Retail Herbal Trade. Adulteration of botanical dietary supplements through the accidental or deliberate use of a plant species other than the one claimed to be present is a well-publicized concern. Recent surveys of these products have found that some historically reported adulterations still occur despite strict quality control regulations. For a few botanicals, the accidental inclusion of toxic lookalike species has caused consumer illnesses. Since most of the Western market, as measured by monetary value, consists of processed dietary supplements, relatively little attention has been paid to the question of whether unprocessed bulk herbs sold to herbalists and in herb stores are equally subject to adulteration. We hypothesized that adulterations similar to those seen in materials sold for use in dietary supplements would occur. Nine botanicals were selected that had been previously reported to be adulterated, or were suspected to be at risk of adulteration, and that could be distinguished from known or likely adulterants by the morphology of parts in commerce. Samples were purchased from eleven vendors and authenticated by morphological examination. Most were correctly identified, and no toxic adulterants were found. Samples of Juniperus and Tilia commonly contained species other than those specified, and most samples of alleged Arnica montana were entirely composed of Heterotheca inuloides (false arnica). We conclude that the likelihood of adulteration of crude botanicals in retail commerce is taxon-specific; while most species are consistently correctly identified, a few are often confused. One implication is that botanicals purchased for use in research should always be independently authenticated in some fashion. Key Words: Adulteration, dietary supplements, herbal medicine, quality control.

Introduction
Adulteration of botanical dietary supplements is a widely publicized problem. Contrary to popular myth, the manufacture and labeling of botanical supplements in the U.S. is subject to strict regulations (Soller et al. 2012). However, as in other industries, some manufacturers illegally adulterate these products either deliberately or through carelessness, occasionally with serious or even fatal health consequences. Finished dietary supplements have repeatedly been reported to contain risky pharmaceutical drugs and drug analogs, with certain categories of product partic-

Received 10 April 2012; accepted 4 September 2012; published online ___________

ularly likely to be adulterated (e.g., Chen et al. 2010; Gryniewicz et al. 2009; Low et al. 2009); excessive heavy metal content is also a potential concern for certain products (e.g., Cooper et al. 2007; Saper et al. 2004). At the stage when unprocessed botanicals are purchased by wholesalers, the most likely form of adulteration is the inclusion, in whole or in part, of undesired species. Substitution of toxic plant species for non-toxic species has occasionally been reported, e.g., in the substitution of Atropa belladonna L. for Arctium lappa L. (Bryson et al. 1978), Digitalis lanata Ehrh. for Plantago major L. (Slifman et al. 1998), Illicium anisatum L. for Illicium verum Hook. f. (Garzo Fernndez et al. 2002; Johanns et al. 2002), and Aristolochia fangchi Y.C. Wu ex L.D. Chow & S.M. Hwang for Stephania tetrandra S. Moore (Koh et al.

Economic Botany, XX(X), 2012, pp. 17 2012, by The New York Botanical Garden Press, Bronx, NY 10458-5126 U.S.A.

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2006). The inclusion of Teucrium species (germander, probably hepatotoxic in some users) in Scutellaria lateriflora L. (skullcap) products continues to occur to this day (Sun and Chen 2011). These adulterations are almost always unintentional, unless the two species are considered under some traditional approach to be substitutable, as for Stephania versus Aristolochia. Much more common, and more often deliberate, are economic adulterations with cheaper or more easily obtained species that, though not known to be toxic, are sometimes likely to be less effective. Many or most of these adulterations could be detected by careful inspection at the time of purchase of unprocessed materials. In todays market, most botanicals are processed into powders or extracts before sale to the manufacturers of finished products, who often do not themselves handle unprocessed botanicals and have no opportunity to authenticate them by morphology. Most recent studies relating to adulteration have therefore dealt with chemical methods of authenticating processed botanicals, whether finished products on store shelves or wholesale material purchased by manufacturers. However, some unprocessed or moderately processed (e.g., cut and sifted) botanicals are diverted to the retail market, where they are available at specialty herb shops and through Internet sales. Bulk herbs may be preferred by some consumers for their lower price, quality, unaltered composition, and/or flexibility of use. Access to these raw botanicals is essential for an herbalist or other knowledgeable consumer who wishes to make a mixture or product type that is not commercially available. Researchers studying medicinal plants also sometimes purchase crude botanicals so that they can make their own extracts using known, controllable, and replicable methods, which they believe will provide some guarantee of quality in their test substances. This raises questions about whether the authenticity of unprocessed bulk herbs in the U.S. retail market can be relied upon. We therefore sought to determine whether adulterations previously reported from the supplement market would be found in unprocessed botanicals sold directly to consumers. It is not clear whether the bulk herbs available to consumers and herbalists through retail venues are more or less likely to be adulterated than those that are used in highly processed commercial products. Because this market is small and marginalized in the U.S., compared to the market for dietary

supplements, the question of material quality has attracted relatively little interest. The hypothesis of the present study was that errors similar to those previously reported in the wholesale herb market and in commercial products would also affect whole herbs in the retail market. Contrarily, one might suppose that adulteration would be less likely, as some botanicals are sold in a readily recognizable form, and many of their purchasers (including herb shop owners and practicing herbalists) would be knowledgeable enough about botanicals to notice and complain about conspicuous errors. The present study therefore sought to identify, in unprocessed herbs in the retail market, adulterations comparable to those previously reported in the botanical industry. Its purpose was not to estimate the overall rate or frequency of adulteration in this market across all plant species, but to find instances of adulteration as efficiently as possible, presuming that they were there to be found. The study design deliberately maximized the likelihood of observing adulteration by not surveying the many botanicals that would have been identifiable by morphology but lacked known or likely adulterants. Results are therefore not generalizable to the entire retail herb market.

Material and Methods


To facilitate identification of potential botanical adulterants, a short list of botanicals for study were selected according to the following criteria: (1) intact material of the parts used in commerce retains enough morphological characters to adequately authenticate the species; (2) the species was available in an unprocessed or minimally processed form from multiple vendors; (3) the species has been reported to be adulterated, or related species that could potentially be confused with it are used commercially or occur in the same region where it is wild-harvested. Because plant species are defined by morphology, morphological identification is the most rigorous possible means of identification, if the available material suffices to permit it. Also, examination of morphological and organoleptic characters (e.g., taste, fracture) is the only means of authenticating purchased material that is available to herb stores and herbalists. However, some isolated plant parts cannot be unambiguously identified by morphology; for example, many roots or barks are not identifiable to the species level, and if they are

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finely cut, admixture of a second species can be virtually impossible to detect. This study excluded botanicals with known adulterants that we did not believe we would consistently be able to distinguish from the genuine article. Nine botanicals were ultimately selected for sampling (Table 1). Botanicals identified by a common name may encompass more than one species, with different species being permitted in commerce in different countries. Since material was purchased on the U.S. market, the circumscription favored in the U.S. was used (Standardized Common Names are given in Table 1 following McGuffin et al. 2000). Eleven herb vendors were chosen, including two shops in the state of Missouri that were physically visited and nine in other states that offered online sales. Geographic distribution of the latter represented several regions of the U.S., with home states including Arizona, California, Colorado,
Table 1. POTENTIALLY
Botanical product

Kentucky, Minnesota, New Hampshire, Oregon, and Pennsylvania. Retailers were assigned code numbers so that reported results would not be associated with a specific retailer. All selected species that were available were purchased from each retailer. Some of these shops may have obtained bulk plant materials from the same wholesalers. No vendor was willing to tell us, when we identified ourselves as researchers interested in purchasing herbs from multiple sources, who their wholesalers were. Thus, it is possible that a single source of adulteration could have given rise to multiple scored instances of adulterated samples received from stores that are widely separated geographically. If so, we believe that the results fairly reflect the actual state of the market. Our interest is not in how many batches of adulterated material were produced, which was impossible to determine, but in how likely it is that a U.S.based researcher

ADULTERATED, BOTANICALLY IDENTIFIABLE HERBS, WITH STANDARDIZED COMMON NAMES AND ALLOWABLE SPECIES FOLLOWING MCGUFFIN ET AL. (2000).

Allowable species

Potential adulterants

Arnica, flowering heads

Chamomile, flowering heads

Arnica montana L. or North American species A. chamissonis Less., A. cordifolia Hook., A. latifolia Bong., A. montana L., A. sororia Greene Matricaria chamomilla L.

Several species of Asteraceae, particularly Heterotheca inuloides Cass. (Wichtl 2004)

Hawthorn, fruit

Crataegus laevigata (Poir.) DC., C. monogyna Jacq., C. piperi Britton, C. rivularis Nutt. Juniperus communis L. Tilia cordata Mill, T. platyphyllos Scop., T. vulgaris Hayne Hypericum perforatum L. Schisandra chinensis (Turcz.) Baill., S. sphenanthera Rehder & E. H. Wilson Scutellaria lateriflora L.

Juniper, pseudofruit Linden, flowers with inflorescences St. Johns wort, herb Schisandra, fruit

Anthemis species, which are likely to be responsible for most reports of allergic reactions (Hausen et al. 1984; Menz and Winkelmann 1987; Wichtl 2004; Youngken 1943) Other species of Crataegus, including those legally sold in Europe or Asia as hawthorn or sold in the U.S. under other common names (McGuffin et al. 2000; Wichtl 2004) Other species of Juniperus (Wichtl 2004) Other species of Tilia (Wichtl 2004) Other species of Hypericum (Wichtl 2004) Potentially confusable with other Schisandra species Teucrium canadense L. (Anonymous 1985; Sun and Chen 2011), a close relative of which is hepatotoxic in some users (Larrey et al. 1992) and which is suspected itself to be toxic Illicium anisatum L., which is toxic (Garzo Fernndez et al. 2002; Johanns et al. 2002; Small 1996; Wichtl 2004)

Skullcap, herb

Star anise, fruit

Illicium verum Hook. f.

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or consumer purchasing one of these species would be supplied with adulterated material. Botanical samples received were examined morphologically with the aid of a hand lens and dissecting microscope to confirm the presence of morphological characters expected in the claimed species and the absence of characters that would be expected only in known or potential adulterants. Morphological and organoleptic characters pertaining to the species of interest and reported adulterants were determined by reference to pharmacognostic compilations (Applequist 2006; Wichtl 2004; Youngken 1943) and taxonomic literature. Presence of more than a very small amount of material having characters not consistent with the stated identity was scored as adulteration; however, the proportion and taxonomic identity of adulterants were taken into consideration in evaluating the potential economic or health effect of the adulteration. Stated identity was defined by the text on the package label. If only a common name was given, all species permitted to be sold under that Standardized Common Name in the U.S. according to Herbs of Commerce (McGuffin et al. 2000) were acceptable for inclusion, whereas if a scientific name was given, the material was expected to belong to that species. Samples of all purchased materials were retained at the Missouri Botanical Garden (MO) to serve as vouchers.

Results and Discussion


Results are summarized in Table 2. For five of the nine selected botanicals, no adulteration was
Table 2. AUTHENTICATION

detected in any examined samples. These include the species that were of most concern due to historical reports of toxic or potentially allergenic adulterants (Scutellaria lateriflora, Illicium verum, and Matricaria chamomilla). The absence of repeatedly reported toxic or even poisonous adulterants in skullcap and star anise is certainly a positive finding. However, since a recent study has reported that four of 13 skullcap supplements contained Teucrium canadense L. (Sun and Chen 2011), and since the authors have seen a recent sample of commercial skullcap, not included within this study, that was over 50 % Teucrium, it is evident that adulteration of Scutellaria lateriflora does remain a serious concern and a potential risk to health. A sixth botanical, schisandra, requires more detailed interpretation. Two species, Schisandra chinensis and S. sphenanthera, are used interchangeably in Chinese medicine (Chen and Chen 2004; Pharmacopoeia Commission of PRC 1997) and both may be sold as schisandra in the U.S. (McGuffin et al. 2000). Our schisandra samples displayed great variation in fruit size; the largerfruited samples were identified as S. chinensis, while four samples having very small, reddishbrown fruits were consistent with S. sphenanthera. Three of the samples that fell into the latter category were labeled only, and appropriately, as schisandra, whereas one was additionally stated on the label to be Schisandra chinensis and was therefore scored as being adulterated. Although the bioactivity of the two species is not known to differ, correct botanical identification may be

OF BOTANICALS OBTAINED FROM U.S.-BASED RETAIL OUTLETS. OK = IDENTITY CONSISTENT WITH CLAIMS ON PACKAGE; * = ADMIXTURE OF A MINORITY OF AN ADULTERANT; X = MOSTLY OR ENTIRELY THE WRONG SPECIES (SEE TEXT FOR FURTHER DETAILS); N/A = BOTANICAL NOT AVAILABLE FROM THAT VENDOR.

VENDOR

Arnica

Chamomile

Hawthorn

Juniper

Linden

St. Johns Wort

Schisandra

Skullcap

Star Anise

1 2 3 4 5 6 7 8 9 10 11

X X OK X OK n/a X X OK X OK

OK OK OK OK n/a OK OK OK OK OK OK

n/a n/a OK OK OK OK OK OK OK OK n/a

* * X * * OK OK X X OK n/a

X OK X X X OK X X OK X n/a

OK OK OK OK OK OK OK OK n/a OK n/a

OK n/a OK OK OK OK X OK OK OK OK

OK OK OK OK OK OK OK OK OK OK n/a

n/a OK OK OK n/a OK OK OK OK OK OK

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important to some purchasers, e.g., those conducting pharmacognostic research, and label claims are legally required to be accurate. For the three remaining botanicals in this study, a majority of samples were adulterated at least in part. Juniper frequently included some admixture of fruits appearing inconsistent with J. communis. This is unsurprising, since juniper is often collected from the wild, where it may occur sympatrically with other species. It is likely that inclusion of a small amount of some other species is consistent with longstanding traditional practice and has little effect on quality. Linden flower and inflorescence usually included material consistent with species of Tilia other than the officially used three; a species having densely hairy bracts was the most common adulterant. The most thorough European reference on the subject indicates that both of these adulterations are not uncommon (Wichtl 2004). Finally, six of ten samples sold as arnica (including one implausibly stated to be Arnica montana of Mexican origin) consisted wholly of another species identified as Heterotheca inuloides, whose substitution for arnica is a persistent quality control problem (Pietta et al. 1994; Wichtl 2004; Youngken 1943); genuine and adulterated samples are shown in Figs. 1a and b. Substitution may be economically motivated, as Heterotheca is a larger and, within its native range, more abundant and accessible plant, but honest confusion might also play a role. Though the Standardized Common Name for H. inuloides in the U.S. is false arnica (McGuffin et al. 2000), in its native Mexico it is usually called simply arnica, and arnica is usually used to mean Heterotheca (Estrada Lugo et al. 1995; Gonzlez Elizondo et al. 2004; Martinez 1969; Moreno Uribe 2004). The two genera have similar traditional uses, especially for bruises (Estrada Lugo et al. 1995; Martinez 1969) but Heterotheca is also consumed as a tea for internal inflammations (Gonzlez Elizondo et al. 2004; Moreno Uribe 2004) and lacks reported toxicity. Although mislabeling is illegal and unacceptable, knowledgeable consumers might rationally prefer false arnica probably safer, cheaper, and more sustainable to the genuine article. Perhaps this particular adulteration has been able to remain common for generations in part because many buyers do not care whether it occurs and would not bother to look for it or to complain if they observed it. It is not known whether the same frequency of adulteration

Fig. 1. a. Authentic arnica (Arnica montana). b. Heterotheca inuloides sold as arnica.

may be found in commercial arnica products at present. Although manufacturers of finished dietary supplements often do not purchase botanically identifiable material, they are legally required to use some means of authenticating their raw materials, and the two genera are readily distinguished chemically. We conclude that the likelihood of economic adulteration of bulk herbs in the retail market is taxon-specific. Some plants that have previously known adulterants were never found to be adulterated, yet a few were frequently adulterated. Accidental or deliberate admixture of related species may be most likely to persist among species that are commonly wild-collected. For effective quality control of bulk herbs, retailers need access to up-to-date information on which species may be problematic, coupled with a general awareness that quality control by wholesalers cannot always be relied upon. Research studies using commercial herbs should always supply some form of independent confirmation of identity or chemical composition. Voucher samples for pharmacognostic studies cannot simply be bagged and stored, but must be subjected to

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botanical identification, chemical fingerprinting, or some other means of authentication. The potentially-adulterated botanicals examined in this study were identifiable using traditional morphological methods which, along with organoleptic methods (e.g., taste, odor, fracture), are the only methods accessible to herbalists or owners of herb shops. Such vendors also typically handle some botanicals that cannot be definitely distinguished from related species by appearance and sensory characteristics, such as powdered herbs and many cut barks and roots. It is possible that, within the subset of botanicals that have known adulterants, such difficult-to-authenticate materials could be more frequently adulterated than those in this study, for which errors are more easily caught. If a morphologically unrecognizable botanical is purchased for use in finished dietary supplements, the manufacturer is required to perform (sometimes repeatedly) chemical or molecular tests to confirm its identity, whereas if it is sold to a retail vendor of unprocessed herbs, that vendor does not have similar tests performed, which would intolerably inflate the retail cost of bulk herbs. If a wholesaler is careless or dishonest, therefore, misidentified material directed towards the retail herb market might be more likely to reach consumers than material that enters the dietary supplement processing stream. Though the adulterations observed in this study were not dangerous, they do point out the risk that inadequate concern for authentication of material by vendors of bulk herbs could lead to the accidental sale of potentially harmful herbs under the wrong name.

Acknowledgments
We thank Dr. John Pruski for helpful advice regarding identification of samples of Asteraceae, and Robert Fuqua for photographs of samples.

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